Volume 10, Issue 2 (2015)
published March 2015
Contents | |
Research articles |
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Xavier Pochon, Javier Atalah, Susanna A. Wood, Grant A. Hopkins, Ashleigh Watts and Christian Boedeker
Cladophora ruchingeri (C.Agardh) Kützing, 1845 (Cladophorales, Chlorophyta): a new biofouling pest of green-lipped mussel Perna canaliculus (Gmelin, 1791) farms in New Zealand
(pp 123-133)
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Cladophora is a genus of branched filamentous green algae (Ulvophyceae). It contains many species that are challenging to differentiate based
on morphology because of the scarcity of diagnostic characters and extensive phenotypic plasticity. Within the past five years, Cladophora
blooms have been observed on the ropes of green-lipped mussel farms in the Marlborough Sounds, New Zealand. When Cladophora reaches high biomass,
it can clog mussel-harvesting equipment; thus, it is considered a nuisance organism in the region. This study used morphological and molecular techniques
to identify the species responsible for the blooms, and to investigate whether this might be a recent incursion. Cladophora samples (n = 21) were
collected from nine mussel farms, one salmon farm, and a marina. Morphological and phylogenetic analyses (partial large subunit and internally transcribed
spacer regions 1 and 2 of the nuclear ribosomal cistron), revealed the identity of the bloom forming species as Cladophora ruchingeri (C.Agardh)
Kützing, 1845. This represents the first report of this species in the Southern Hemisphere and Pacific region. Given the distinct morphology of C. ruchingeri
(when mature), its absence from previous surveys of macro-algae from this region, and increasing reports of blooms, our findings suggest that this species has
only recently been introduced to New Zealand. This study provides a robust taxonomic identification and initial baseline data. Further directed studies
on Cladophora are required to advance knowledge on its ecology and distribution in New Zealand, and assist in the development of mitigation strategies.
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Collin H. Johnson and Robert M. Woollacott
Analyses with newly developed microsatellite markers elucidate the spread dynamics of Tricellaria inopinata d’Hondt and Occhipinti-Ambrogi, 1985 - a recently established bryozoan along the New England seashore
(pp 135-145)
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The majority of bryozoans possess short-lived larvae with limited dispersal potential, yet many species of bryozoans have obtained global distributions.
The marine bryozoan Tricellaria inopinata d’Hondt and Occhipinti-Ambrogi, 1985 was first described from specimens collected in 1982 in the Lagoon of Venice,
but is thought to be native to the northeast Pacific. By 2009, it could be found in various locales in the eastern Atlantic including Spain, France, England, and Ireland.
In 2010, T. inopinata was found for the first time in the western Atlantic in Eel Pond, Woods Hole, Massachusetts, and shortly thereafter was collected in several
other locales in the area. A newly developed suite of polymorphic microsatellite loci was used to investigate this recent range expansion of T. inopinata
in an effort to understand what makes these animals such successful invaders. We examined various aspects of the population genetics of adult colonies collected
from four sites in eastern Massachusetts: Eel Pond, Boston Harbor, Marblehead and Gloucester. There was significant genotypic differentiation between all sites.
Higher homogeneity between the Eel Pond and Boston Harbor populations, as well as the potential for Eel Pond acting as a source of migrants for Boston Harbor,
suggest that Eel Pond was a source population for the Boston Harbor population. In contrast, levels of genotypic differentiation and a lack of migrants suggested
that the Marblehead and Gloucester populations likely did not originate from animals in Eel Pond. Thus, the recent range expansion by T. inopinata
in the western Atlantic appears to be a result of multiple introduction events.
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Robert Hershler, Hsiu-Ping Liu, James T. Carlton, Andrew N. Cohen, Cheryl B. Davis, Jeff Sorensen and David Weedman
New discoveries of introduced and cryptogenic fresh and brackish water gastropods (Caenogastropoda: Cochliopidae) in the western United States
(pp 147-156)
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We report the discovery of a second western Atlantic brackish-coastal cochliopid gastropod in San Francisco Bay (Spurwinkia salsa (Pilsbry, 1905)),
and detail the first records for a widely distributed member of the family, Tryonia porrecta (Mighels, 1845), from artificial lakes (in the Phoenix
metropolitan area). These identifications were based on morphological criteria and supported by mitochondrial DNA sequence data that also indicates little
or no divergence of the newly reported populations, which is consistent with evolutionarily recent spread or separation. Spurwinkia salsa was most
likely introduced to San Francisco Bay either in recent decades in bait worm packing or ships’ ballast or in the 19th or early 20th century in solid ballast
or with oyster imports. The discovery of T. porrecta in artificial lakes in the Phoenix area in 1984 and 2014 may be due to either recent arrival
in the area or to dispersal into a newly available habitat from a population long present in the area. In either case, the occurrence of T. porrecta
in the Phoenix area is likely due to transport on birds along an eastern branch of the Pacific Flyway. The discovery of T. porrecta in artificial
lakes suggests that this species (which is typically distributed in thermal springs) is more broadly tolerant than previously thought. Additional spread
of this unusual snail within the highly modified aquatic ecosystem of the Phoenix metropolitan area (which includes more than 900 artificial lakes) would
appear likely.
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Luiz Eduardo Macedo de Lacerda, Caroline Stahnke Richau, Cesar R.L. Amaral, Dayse Aparecida da Silva, Elizeu Fagundes Carvalho and Sonia Barbosa dos Santos
Ferrissia fragilis (Tryon, 1863): a freshwater snail cryptic invader in Brazil revealed by morphological and molecular data
(pp 157-168)
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The results of our study confirm the occurrence of the cryptic invader Ferrissia fragilis (Tryon, 1863) in Brazil, a species of worldwide geographical
distribution and with poorly known morphology that is pervasive in several countries. Specimens were collected in the states of Rio de Janeiro and Minas Gerais
in southeastern Brazil. We describe their morphology, and analyze the similarity of haplotypes generated from these samples with those previously obtained for
F. fragilis. Shell morphology was compared by light and scanning microscopy. Soft parts of stained dissected specimens were studied under
the stereomicroscope. Molecular analysis was performed on three specimens from each sample using the mitochondrial cytochrome c oxidase I gene.
Based on a comprehensive analysis, including both morphological and molecular methodologies, we were able to identify the examined specimens as F. fragilis.
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Brittany Harried, Kyle Fischer, Kathryn E. Perez and Gregory J. Sandland
Assessing infection patterns in Chinese mystery snails from Wisconsin, USA using field and laboratory approaches
(pp 169-175)
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The success of invasive species establishment in new habitats depends, in part, on interactions with other members of the invaded community.
Cipangopaludina chinensis, the Chinese mystery snail (CMS), is an exotic, invasive snail in North America. Since its introduction in the 1890s,
CMS have spread to a number of watersheds across the United States and parts of Canada. This invasion has generated questions about the snail’s capacity
to serve as a host for parasites within local habitats, including parasites with conservation implications. To begin addressing these questions, we necropsied
147 wild-caught snails from 22 lakes across Wisconsin, finding only two CMS individuals harboring trematode (flatworm) parasites. We also conducted experimental
exposures using a trematode (Sphaeridiotrema pseudoglobulus) implicated in waterfowl die-offs and found that CMS infection levels were significantly lower
than those in co-occurring snail species. Furthermore, the parasites that did successfully infect CMS were often found encased in the shells of the snails
in a non-viable state. Together these results 1) provide insight into the importance of CMS as a host for parasites in the region, and 2) may help to explain
the wide distribution of CMS across WI and the Midwest.
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Niels-Viggo Hobbs, Eric Lazo-Wasem, Marco Faasse, Jeffery R. Cordell, John W. Chapman, Carter S. Smith, Robert Prezant, Rebecca Shell and James T. Carlton
Going global: The introduction of the Asian isopod Ianiropsis serricaudis Gurjanova (Crustacea: Peracarida) to North America and Europe
(pp 177-187)
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The Asian isopod Ianiropsis serricaudis is now well established in fouling communities, often associated with introduced ascidians,
throughout the Northern Hemisphere but has gone largely unnoticed because of its diminutive size (typically less than 3 mm in length) and
the difficulties of identifying small peracarid crustaceans. Known locations include the northeastern Pacific (Puget Sound, San Francisco Bay,
and Monterey Bay), the northwestern Atlantic (from the Gulf of Maine to Barnegat Bay, NJ), and the northeastern Atlantic (England and the Netherlands).
We predict that this species is widespread along North America and European coasts, and may already be introduced to cold temperate waters
of the Southern Hemisphere as well.
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Scott M. Reid and Joseph J. Nocera
Composition of native crayfish assemblages in southern Ontario rivers affected by rusty crayfish (Orconectes rusticus Girard, 1852) invasions – implications for endangered queensnake recovery
(pp 189-198)
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Orconectes rusticus (rusty crayfish) is an aggressive and prolific aquatic invader. Where introduced, it has caused dramatic ecosystem changes,
including the replacement of native crayfishes. In Canada, it was first reported in Lake of the Woods in northwestern Ontario and a small number
of south-central Ontario lakes during the 1960s. It has subsequently spread to other regions of the province. Its current expansion into southwestern
Ontario rivers presents an unknown risk to the endangered queensnake (Regina septemvittata), an obligate feeder on freshly molted crayfish. We sampled
99 river sites across southern Ontario to: (i) describe crayfish assemblages within river reaches currently occupied by Queensnake; and, (ii) characterize
the impact of O. rusticus on native crayfish assemblages. O. rusticus was caught at 41% of sites sampled, and was the only species at 24% of sites.
The abundance, richness, and within-site distribution of native crayfishes were all significantly lower at sites with O. rusticus. Within the distribution
of queensnake, crayfish assemblages were almost entirely dominated by O. propinquus, with O. rusticus being absent. However, O. rusticus was
found along the lower Speed River, where only one dam separates it from Grand River queensnake populations. Given its past spread, O. rusticus will likely
be introduced into areas used by queensnake and replace O. propinquus (the primary prey of queensnake). The adaptability of queensnake to prey upon non-native
crayfish is unknown and requires investigation.
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Luca Peruzza, Federica Piazza, Chiara Manfrin, Lucrezia Celeste Bonzi, Silvia Battistella and Piero Giulio Giulianini
Reproductive plasticity of a Procambarus clarkii population living 10°C below its thermal optimum
(pp 199-208)
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In this study the annual reproductive biology of a Procambarus clarkii (Girard, 1852) population living in an atypical habitat with cold spring waters
is investigated by monitoring Gonado-Somatic and Hepato-Somatic Indexes (GSI and HSI) and by performing cytology on ovaries. Despite its known preference
for habitats with water temperature from 21 to 30 °C, our results clearly confirm the adaptation of this population to the atypical thermal habitat,
characterised by an annual mean water temperature value of 13.32 ±0.08 °C. Maximum gonadal development was reached in August, with maximum GSI median
value of 0.64 (instead of reported values even 10 times higher for other populations), and ovigerous females were found in autumn, with mean realized
fecundity of 35 ±7 compared to 285–995 reported from other habitats. Histological analysis was consistent with other studies and allowed us to follow
ovarian development at cytological level. The importance of all these results is not to be underestimated: to our knowledge these findings are the first
report of the coolest habitat successfully colonized by this species at the present time and so they have to be taken as a warning about the possible range
expansion of P. clarkii also to northern and colder habitats that have few things in common with the native habitat of the species and, up to now,
were considered “safe” from the invasion of the red swamp crayfish.
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Stefania Chiesa, Massimiliano Scalici, Livia Lucentini and Francesco Nonnis Marzano
Molecular identification of an alien temnocephalan crayfish parasite in Italian freshwaters
(pp 209-216)
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Although the symbionts of non-vertebrate metazoans have received scarce attention, scientific interest has recently increased as these symbionts
can spread diseases and alter the diversity of the ecosystem where hosts are introduced. We report here a symbiont newly described by molecular
markers and observed on the yabby Cherax destructor Clark, 1936, collected in Italian freshwaters. Preliminary morphological observations were
performed and a species identification was proposed using molecular techniques. In particular, a 644-bp long 28S rDNA fragment was successfully
sequenced and could be aligned for the entire sample set. The minimum spanning network identified two haplotypes clustered into a single haplogroup
(H1) together with Temnosewellia minor Haswell, 1888 reference sequences. Considering the introduction of temnocephalans, this represents the third
discovery of alien crayfish symbionts in Italian freshwaters, but the first obtained by molecular data. Outside Europe, there are only few records
of alien temnocephalans worldwide, introduced with the crayfishes from Australia. The occurrence of this new temnocephalid species and the great number
of potential hosts species inhabiting Italian freshwaters suggest that the Italian peninsula might have many undescribed temnocephalid populations/species.
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Michael E. Guinan Jr, Kevin L. Kapuscinski and Mark A. Teece
Seasonal diet shifts and trophic position of an invasive cyprinid, the rudd Scardinius erythrophthalmus (Linnaeus, 1758), in the upper Niagara River
(pp 217-225)
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Dietary shifts of invasive rudds Scardinius erythrophthalmus (Linnaeus, 1758) and food web structure of the upper Niagara River were examined.
Stable isotope analysis (SIA) of liver tissue was used to test the hypothesis that rudds shifted their diets from piscivory during early spring months
when macrophyte availability was low towards herbivory when macrophytes were abundant and warmer water temperatures facilitated digestion. Muscle tissue
was used to evaluate the trophic position of rudds and other invasive species relative to native species. SIA revealed enriched δ15N and depleted δ13C
in liver tissue of rudds during early spring months, suggesting a mostly piscivorous diet of pelagic origin when macrophyte availability was low,
and depressed δ15N and elevated δ13C values during warmer summer months when littoral macrophytes were abundant. Analysis of muscle tissue from late
summer indicated that rudds and other invasive fishes, including common carp Cyprinus carpio (Linnaeus, 1758) and goldfish Carassius auratus (Linnaeus, 1758),
had similar trophic positions that may be attributed to their omnivorous feeding strategies. The ability of rudds to shift their diets from feeding
on fishes of pelagic origin towards consuming littoral macrophytes is an adaptation that is likely to both facilitate invasion and create novel pathways
of nutrient transfer among habitat types. Our results provide an increased understanding of the feeding ecology of the rudd and the role of this invasive
species in the food web of the upper Niagara River.
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Kristína Hôrková and Vladimír Kováč
Ontogenetic phenomena, temporal aspect, and ecological factors in the successful invasion of round goby Neogobius melanostomus in the River Danube
(pp 227-235)
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Plasticity in life-history traits is thought to be one of the key factors that contribute to adaptation of invasive species to the novel environment
at the beginning of an invasion. It has been found that round gobies Neogobius melanostomus from freshly invaded areas (invasion front) exhibit
different life-history traits than individuals from core or central areas with well-established populations. The theory of alternative ontogeny and
invasive potential predicts such differences. Nevertheless, it is difficult to distinguish between the effects of intrinsic ontogenetic phenomena
and the effects of particular ecological factors on life-history traits of populations at various stages of invasion. Thus, the main aim of this study
was to test the prediction that two sub-populations of round gobies from two habitats exposed to a different intensity of anthropogenic pressures
in the River Danube, but at the same stage of invasion, will have significant differences in their reproductive parameters. Females from the relatively
undisturbed habitat were predicted to have 1) larger oocytes, 2) lower absolute number of oocytes, and 3) lower real absolute fecundity. For two parameters
(1 and 3), differences were statistically significant, as predicted. For parameter 2, the difference was as predicted, though not significant. Several
studies suggest that changes in life-history traits observed over the progressing invasions of fishes are typical rather than accidental. They appear
to be related to the stage of the invasion and closely associated with ontogenetic phenomena (the capability to generate alternative ontogenies).
However, ecological factors also play an important role in this process. If the habitat is exposed to permanent disturbances, the established invasive
population will probably keep the same life-history traits as at the beginning of the invasion.
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Tiffany S. Garcia, Jennifer C. Rowe and James B. Doyle
A tad too high: Sensitivity to UV-B radiation may limit invasion potential of American bullfrogs (Lithobates catesbeianus) in the Pacific Northwest invasion range
(pp 237-247)
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Biological invasion potential can be strongly influenced by abiotic factors such as temperature, water availability, and solar radiation.
Invasive species that possess phenotypically plastic traits can mediate impacts from these stressors, but may be unable to recognize and respond to dangerous
levels in a novel environment. Understanding potential constraints on appropriate trait responses induced by abiotic stressors can aid in the management and
control of important invaders. Our study explored tolerance and plastic trait response to UV-B radiation in an invasive anuran, the American bullfrog
(Lithobates catesbeianus Shaw, 1802). We experimentally quantified larval mortality rates and color change responses across two larval size classes.
In a second experiment, we investigated the potential for a correlated color change and behavioral (refuge use) response in the small size class. We predicted
that individuals would respond to stressful and potentially harmful UV-B exposure rates with darkening of body coloration, and when refuge was available,
a correlated defense strategy utilizing both color change and refuge. We found an increase in larval mortality across both size classes at UV-B exposure rates
typical to both low and high elevation aquatic breeding sites (10-12µW/cm² and 20-24µW/cm², respectively). Only bullfrog larvae in the small size class exhibited
a darkening in body color when exposed to high UV-B treatments. Although this smaller size class did exhibit color plasticity, individuals did not correlate changes
in body coloration with changes in refuge use. These results suggest ontogenetic differences (estimated by size class) in plastic color response to UV-B stress
as well as constraints on behavioral use of refuge. These findings are important in understanding differences in bullfrog occupancy of breeding habitats across
an elevational gradient, particularly in Oregon’s Cascade Mountain Range, where bullfrog distributions are currently limited at elevations above 1000m.
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